Genomic analysis of the regulatory elements and links with intrinsic DNA structural properties in the shrunken genome of Buchnera

Abstract

BackgroundBuchnera aphidicola is an obligate symbiotic bacterium, associated with most of the aphididae, whose genome has drastically shrunk during intracellular evolution. Gene regulation in Buchnera has been a matter of controversy in recent years as the combination of genomic information with the experimental results has been contradictory, refuting or arguing in favour of a functional and responsive transcription regulation in Buchnera.The goal of this study was to describe the gene transcription regulation capabilities of Buchnera based on the inventory of cis- and trans-regulators encoded in the genomes of five strains from different aphids (Acyrthosiphon pisum, Schizaphis graminum, Baizongia pistacea, Cinara cedri and Cinara tujafilina), as well as on the characterisation of some intrinsic structural properties of the DNA molecule in these bacteria.ResultsInteraction graph analysis shows that gene neighbourhoods are conserved between E. coli and Buchnera in structures called transcriptons, interactons and metabolons, indicating that selective pressures have acted on the evolution of transcriptional, protein-protein interaction and metabolic networks in Buchnera. The transcriptional regulatory network in Buchnera is composed of a few general DNA-topological regulators (Nucleoid Associated Proteins and topoisomerases), with the quasi-absence of any specific ones (except for multifunctional enzymes with a known gene expression regulatory role in Escherichia coli, such as AlaS, PepA and BolA, and the uncharacterized hypothetical regulators YchA and YrbA). The relative positioning of regulatory genes along the chromosome of Buchnera seems to have conserved its ancestral state, despite the genome erosion. Sigma-70 promoters with canonical thermodynamic sequence profiles were detected upstream of about 94% of the CDS of Buchnera in the different aphids. Based on Stress-Induced Duplex Destabilization (SIDD) measurements, unstable σ70 promoters were found specifically associated with the regulator and transporter genes.ConclusionsThis genomic analysis provides supporting evidence of a selection of functional regulatory structures and it has enabled us to propose hypotheses concerning possible links between these regulatory elements and the DNA-topology (i.e., supercoiling, curvature, flexibility and base-pair stability) in the regulation of gene expression in the shrunken genome of Buchnera.

Systematic discovery of uncharacterized transcription factors in Escherichia coli K-12 MG1655

“…This failure to identify binding sites could have happened for two reasons: (i) our conditions did not activate these TFs (e.g., YagI was recently identified as a regulator of xylonate catabolism using the SELEX method in vitro ( 77 )); and (ii) current prediction algorithm methods may generate false-positive candidates. Recently, the annotations of YihY and YchA have been updated to putative inner membrane protein and transglutaminase-like/TPR repeat-containing protein, respectively, though their physiological functions remain unclear ( 3 , 78 ). However, it is still necessary to develop a systematic workflow to predict and validate TFs and improve our knowledge of the TRN.…”

Order from the Order: How a Spatiotemporal Genetic Program Is Encoded in a 2-D Genetic Map of the Bacterial Chromosome

“…Whereas previous studies suggested a particular order of genes in the circular bacterial chromosome [Rocha and Danchin, 2003], recently a striking order of gene arrangement was observed in bacteria along the axis of chromosomal origin (OriC) and terminus (Ter) of replication Muskhelishvili [Brinza et al, 2013;Sobetzko et al, 2012]. In E. coli , the genes required for fast growth, including the replication initiation gene dnaA , the atp operon encoding the major ATP synthase required under aerobic conditions, the gyrB gene encoding the GyrB subunits of DNA gyrase and the ribosomal RNA operons, as well as their activator fis , are located near OriC, whereas the genes needed at later stages, including the DNA relaxing topoisomerases, the regulator of anaerobic metabolism fnr and the genes of NAPs produced on transition to stationary phase (e.g.…”

Coherent Domains of Transcription Coordinate Gene Expression During Bacterial Growth and Adaptation

“…The former is enriched in anabolic genes and the latter in catabolic genes [71]. More compellingly, the temporal expression of genes is tightly coupled to their spatial arrangement in the chromosome-a feature that is conserved in both the γand the α-proteobacteria [61,72]. Thus, in E. coli, the spatial order of genes along the chromosomal OriC-Ter axis and the temporal expression of genetic function is coupled with a strategic organization of sequences with distinct thermodynamic stability around the opposite chromosomal poles.…”